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First published online June 27, 2008
Journal of Experimental Biology 211, 2243-2251 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016147
The contribution of axial fiber extensibility to the adhesion of viscous capture threads spun by orb-weaving spiders
Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
* Author for correspondence (e-mail: bopell{at}vt.edu)
Accepted 28 April 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: orb-web, prey capture thread, thread adhesion, viscous thread
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Eberhard,
1986; Eberhard,
1989; Eberhard,
1990). Viscous threads are spun from the spigots of two adjacent
silk glands (Foelix, 1996).
The flagelliform glands produce a pair of supporting axial fibers, and the
aggregate glands coat these fibers with a viscous, aqueous solution that
quickly forms into droplets (Peters,
1986; Peters,
1995; Vollrath et al.,
1990). The glycoprotein granules that coalesce inside each droplet
contribute to thread adhesion (Vollrath
and Tillinghast, 1991;
Tillinghast et al., 1993) and
the hydrophilic compounds in the surrounding fluid attract atmospheric
moisture to prevent droplets from drying
(Townley, 1990;
Vollrath et al., 1990; Townly
et al., 1991).
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). The viscous
threads produced by members of this clade replaced the cribellar prey capture
threads spun by members of their sister clade, the Deinopoidea
(Coddington, 1986;
Coddington, 1989;
Griswold et al., 1998;
Garb et al., 2006). Cribellar
capture threads are also supported by a pair of axial fibers. However, these
fibers are covered by an outer sheath of fine, dry, looped protein fibrils
(Peters, 1984;
Peters, 1986;
Peters, 1992;
Eberhard and Pereira, 1993;
Opell, 1999) that are drawn
from the spigots of an oval spinning plate, termed the cribellum, by a
spider's calamistrum, a setal comb on the metatarsus of each of its fourth
legs (Eberhard, 1988;
Opell, 2001). Rhythmic
adductions of the median spinnerets press the fibril sheath around the
supporting strands to produce a thread that has a complex, but often regular,
surface configuration (Peters,
1986).
Relative to the volume of material invested in a mm of thread, viscous
threads achieved an average of 13 times more stickiness than cribellar thread
(Opell, 1998). A factor
contributing to the efficiency of viscous thread is its ability to recruit
adhesion from multiple droplets using what Opell and Hendricks have described
as a suspension bridge mechanism (SBM)
(Opell and Hendricks, 2007).
Together, the extensibility of a thread's axial fibers and the plasticity of
its droplets allow it to bow as the thread is pulled away from a contacting
surface. This configuration divides the loading force into perpendicular and
parallel vectors, the latter being responsible for recruiting adhesion for
droplets that lie interior to the edges of a thread's contact with a surface.
As the axial fibers of viscous threads are more extensible than those of
cribellar threads (Blackledge and Hayashi,
2006), viscous threads appear better equipped to implement the SBM
than do cribellar threads. Documentation of this comes from the observation
that viscous thread spans of increasing length register increasing stickiness
(Opell and Hendricks, 2007)
whereas there is no change in the stickiness of cribellar thread spans of
increasing length (Hawthorn and Opell,
2003; Opell and Schwend, in
press).
The present study examines more precisely the contribution of axial fiber extensibility to viscous thread adhesion as it tests the hypothesis that reducing the extensibility of a thread's axial fibers reduces its expressed stickiness. It does so by examining the viscous threads of five araneoid species that have droplet profiles that range from small, closely spaced droplets to large widely spaced droplets (Fig. 1). The stickiness of these threads was first measured under their native tensions and again after they were stretched to two different lengths to reduce the extensibility of their axial fibers. Stretching threads also increases the distance between their droplets (Fig. 2). To maintain the number of droplets that contributed to the stickiness of a thread span, we measured the stickiness of stretched threads with contact plates whose widths were increased in proportion to the degree of thread elongation.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Altering axial fiber extensibility
We collected unstretched capture threads from web-sampling rings using a
microscope slide sampler, made by gluing 4.8 mm square brass supports to
microscope slides at 4.8 mm intervals. Double-sided Scotch® tape (Tape
665; 3M Co., St Paul, MN, USA) on these supports held the threads securely and
maintained their native tensions. Before collecting thread samples, we placed
brass bars with double-sided tape on one surface across the collecting ring's
rim and center bar to isolate web regions. This permitted us to collect a
thread sample from one region of the sampling ring without disturbing threads
in other regions. Next, a set of 4–8 threads (depending on the spacing
of a species' capture spirals) was collected between two 5 mm-wide bars that
were attached to the jaws of a digital caliper in preparation for thread
elongation. Double-sided carbon tape (used for mounting specimens to be
examined with a scanning electron microscope) secured threads to bars. To hold
these threads even more securely, we applied Kores® mimeograph correction
fluid (Ink Technology Corp., Tenafly, NJ, USA) along the length of thread
spans that contacted the tape. This red fluid is a fast-drying paint whose
principal solvent appears to be ether. It immediately adhered to the
double-sided tape and, when dry, formed a thin seal on the tape's surface. We
then slowly separated the jaws of the caliper at a speed of approximately 232
µms–1 to elongate threads and then collected stretched
threads on a microscope slide thread sampler. Threads were elongated to
lengths that corresponded to the widths of the contact plates used to measure
thread stickiness (Fig. 2).
Unstretched threads were measured with contact plates that were 963 µm
wide. One set of threads was stretched 2.215 times their native lengths and
measured with 2133 µm-wide contact plates. Another set of threads was
stretched 3.345 times their native lengths and measured with 3222 µm-wide
contact plates. For simplicity, we refer to these elongations as 1x,
2x and 3x. We examined each of these preparations under a
dissecting microscope so that we could remove damaged threads, eliminate
capture thread spans through which radial threads passed and, in species whose
capture threads were very closely spaced, remove threads to achieve spacing
appropriate for our stickiness measurement procedures. In the process, we were
able to confirm that neither the mimeograph correction fluid or its solvent
bled onto the suspended threads, as the spacing and features of the droplets
near the edges of these threads were indistinguishable from those at the
centers of the threads.
Measuring thread stickiness
As illustrated previously (Opell and
Hendricks, 2007), the instrument used to measure thread stickiness
allowed us to align a microscope slide sampler so that a thread span was
perpendicular to the length of a contact plate. A linear actuator moved thread
spans relative to the contact plate, and a sensitive load cell, to which a
contact plate was connected by a lever system, recorded the force of adhesion
generated as a thread span was pulled from a contact plate. A thread was first
pressed against a contact plate at a speed of 0.06 mm s–1
until a force of 25 µN was generated and was then immediately withdrawn at
the same speed until the thread pulled free of the contact plate. The maximum
force registered by a thread was recorded as its stickiness. For each thread
elongation, we measured the stickiness of three thread sectors using contact
plates of an appropriate width (963, 2133 or 3222 µm) and recorded the mean
of these three measurements as a thread's stickiness value for that thread
elongation. The contact plates were covered with Scotch Magic® tape (Tape
810; 3M Co.), which provided a smooth acetate surface that maximized thread
contact and eliminated the possibility that threads with different droplet
profiles might respond differently to a textured surface. This was the same
material from the same roll of tape used by Opell and Hendricks to document
the operation of the SBM (Opell and
Hendricks, 2007). This acetate was replaced frequently and care
was taken to ensure that each stickiness measurement was made with an unused
sector of a contact plate. Immediately before taking each series of three
stickiness measurements, we recorded laboratory temperature, humidity and
barometric pressure. All measurements of one individual's threads were
completed before measurements of another individual's threads were begun.
Measuring droplet size and spacing
Using techniques described more fully by Opell and Hendricks
(Opell and Hendricks, 2007),
we photographed the threads of each individual spider at each of the three
elongations and measured these digital images with ImageJ (ImageJ, 2006;
http://www.uhnresearch.ca/facilities/wcif/imagej/;
Bethesda, MD, USA) to characterize the size and spacing of their primary
droplets (Table 1). Threads
spun by some individuals also have smaller secondary droplets between some of
their primary droplets (Fig.
1). As these comprise only a small part of the thread's total
volume per mm (A. aurantia 1.9%, A. marmoreus 3.4%, M.
gracilis 4.0%, V. arenata 0.6%, C. turbinata 10.8%;
B.D.O. and M.L.H., unpublished observations) and their presence and size were
variable, we included only the primary droplets in this study. The profiles of
viscous droplets best matched those of a parabola
(Opell and Hendricks, 2007).
Therefore, we determined droplet volume (DV) using the following formula
generated from the formula of a parabola rotated around its x-axis
(Opell and Hendricks, 2007):
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Computing adjusted stickiness per droplet
We first divide the stickiness registered by contact plates of each width
by the number of droplets contacting the plate. Droplet number was computed by
multiplying the DPMM for 1x, 2x and 3x elongated threads by
the width of the 0.963, 2.133 and 3.222 mm-wide contact plates, respectively.
Although this mean stickiness per droplet accounted for most of the effects of
incomplete thread elongation, a minor additional adjustment was necessary to
account fully for the operation of the SBM. In thread spans of increasing
lengths, each additional pair of droplets contributes successively less
adhesion, as less adhesion is recruited from interior droplets than from edge
droplets (Opell and Hendricks,
2007). Consequently, although increasing the number of droplets in
a strand increases the strand's stickiness, it also results in a slight
reduction in the mean stickiness per droplet
(Fig. 4). Thus, our failure to
adequately stretch threads increased the number of droplets that contributed
to a strand's stickiness and this, in turn, slightly reduced the stickiness
per droplet of 2x and 3x elongated threads.
Fig. 4 illustrates this for
threads of C. turbinata, using previous data
(Opell and Hendricks, 2007) to
compute the mean stickiness per droplet (SPD) for unstretched threads measured
with contact plates of 963, 1230, 1613, and 2133 µm widths. It shows that,
as the number of droplets contacting plates of greater widths increases, the
thread span's mean SPD decreases.
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Consequently, it was necessary to correct the SPD values of under-stretched
threads. The relationship between droplet number and SPD described above and
illustrated in Fig. 4 provides
a mechanism for doing so. By knowing how many additional droplets contacted
the plates used to measure the stickiness of 2x and 3x stretched
threads than the plate used to measure unstretched thread, it was possible to
restore the SPD lost to increases in the number of contacting droplets. In the
example of C. turbinata (Fig.
4), insufficient thread elongation resulted in five additional
droplets contributing to the stickiness of the stretched thread. Multiplying
these five additional droplets by the slope of the regression line and adding
this product to the measured mean SPD for the stretched thread yields a value
that we term adjusted SPD (ASPD), which corrects for the slight reduction in
SPD due to the increased number of droplets. We generated similar regressions
for A. marmoreus from data used in Opell and Hendricks
(Opell and Hendricks, 2007)
and for A. aurantia, M. gracilis and V. arenata from data
that were gathered for a broader survey (B.D.O. and M.L.H., unpublished
observations). The regressions for these additional species are:
y=0.0002x+5.1774, y=0.0003x+12.4666,
y=0.0006x+1.8627, and y=0.0011x+11.7829,
respectively, where y is the value added to the measured SPD, and
x is the number of additional droplets contacting a plate used to
measure the stickiness of stretched threads.
Measuring the breaking length of threads
As the native extensibility of viscous threads differs among species
(Opell and Bond, 2001), we
judged that our thread elongation procedure probably did not affect the
extensibility of each species' axial fibers in the same way. To evaluate this,
we measured the breaking lengths of capture threads relative to their native
lengths, using the same caliper apparatus described above, the same methods
for affixing threads to the bars on this caliper's jaws, and the same rate of
elongation to measure the breaking lengths of capture threads. We collected a
series of 3 mm-long thread spans from each web, extended these threads and
recorded the breaking length of each strand. We then computed breaking factor
by dividing a thread's initial length by its length at rupture.
Evaluating breaking factors of threads
Differences in the breaking factors of the five species' threads
(Table 1) indicate that our
elongations did affect their threads differently. When a viscous capture
thread is strained (elongated), its stress initially increases gradually and
then in a more pronounced manner as it enters the stress hardened phase of its
stress–strain curve prior to rupture
(Köhler and Vollrath,
1995; Blackledge and Hayshi,
2006). Thus, at elongations of 3x stretched, the threads of
V. arenata were much nearer their rupture values and were much
stiffer than the 3x stretched threads of the other species. By contrast,
at an elongation of 3x, the threads of M. gracilis were still
quite extensible. Because the analysis of our controlled thread elongations
indicated that some thread slippage occurred during the stretching procedure,
the breaking factors that we report may be inflated. However, if most of this
slippage occurred when stretched threads were transferred from the caliper to
the microscope slide samplers, then these breaking factors are not greatly
inflated. Whichever scenario is correct, we believe that breaking factors are
useful in assessing differences in the residual extensibility of viscous
threads in the five species' orb-webs.
The standard index of a fiber's extensibility is its Young's modulus, with
higher values indicating stiffer fibers. Young's modulus is computed by
dividing stress in MPa by strain, expressed as a percentage of a fiber's
initial length. Thus, a fiber's Young's modulus can be computed at any
elongation from its stress–strain curve. Although we were not equipped
to generate stress–strain curves for threads of the species we studied,
we were able to compute an index that we term `relative Young's modulus' (RYM)
for each species' threads at each of their realized elongations. We based
these values on the stress–strain curve for the viscous capture threads
of Araneus diadematus
(Köhler and Vollrath,
1995). From this curve, we determined the Young's Modulus at the
full range of thread stresses up to and including the thread's rupture value.
We then plotted these values as RYM, where Young's modulus at rupture=1,
against relative thread elongation, where elongation at rupture=1, and
mathematically described this relationship
(Fig. 5). For each elongation
of each individual's threads we computed a relative thread elongation ratio by
dividing the achieved thread elongation by the mean breaking elongation of its
species. We then used the regression formula shown in
Fig. 5 to assign RYM values to
these achieved thread elongations (Table
1, Fig. 6).
Although RYM is more appropriate than thread elongation for describing the
amount of residual extensibility in a thread's axial fibers, it is based on
the thread of a species not included in this study and, therefore, it only
approximates residual thread extensibility. The regression model assigned a
RYM value of 0.083843 to unstretched threads. Although this base value might
be regarded as an artifact of the modeling process, it is probably a
reasonable estimate because threads were already under some tension in the
orb-web and because threads were slightly elongated as their stickiness was
being measured.
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Testing the effects of droplet volume and thread elongation on stickiness
For each individual's threads at each elongation we determined DV, ASPD and
RYM. Within a species, droplet volume is directly related to the stickiness of
viscous threads (Opell, 2002;
Opell and Schwend, 2007),
although this relationship may not be as strong among species
(Opell and Schwend, 2008).
Moreover, our hypothesis predicted that RYM should contribute negatively to
stickiness, as larger values of RYM indicate stiffer threads. We used the SAS
statistical package (SAS Inc., Cary, NC, USA) to test the normality of droplet
volumes, to compare the droplet volumes of threads stretched to different
lengths and to generate regression models that tested the hypothesized
contribution of DV and RYM to ASPD in each of the five species. Data were
considered normally distributed if P>0.05 for a Shapiro–Wilk
W-statistic test. We examined normally distributed data with one-way analyses
of variance (ANOVA) and t-tests (T). Data that were not normally
distributed were compared with Kruskal–Wallis 
2 tests
(KW). We considered regression models with 0.10
P>0.05 to
provide weak support for the hypothesis and P
0.05 to provide
strong support for the hypothesis.
Thread elongation clearly altered the RYM of an individual's thread samples (Fig. 6). Moreover, the range of intraindividual droplet volume of the 1x, 2x and 3x threads was considerable, from 31 to 61%, and averaged 51% of mean individual droplet volume (Table 1). Given these differences, the separate measurements of the RYM, DV and ASPD that we obtained for each individual's 1x, 2x and 3x threads were largely independent of one another. However, there is still the possibility of a spider-specific effect among the three factors (RYM, DV, individual) that contributed to ASPD. Therefore, we report two sets of P values for each species' regression model: P (EDF1), whose F value was computed using an error degree of freedom (EDF) based on the number of individuals sampled, and P (EDF2), whose EDF was based on a sample size reduced by one-third to account for any effect of measuring the threads of individuals at three elongations. Thus, EDF2 provides a more conservative test of the hypothesis by diminishing the individual component through reduced F values and increased P values.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In M. gracilis, V. arenata and C. turbinata, DV and RYM jointly explained ASPD in models judged on both full and reduced EDF values (Table 3). In these three species, DV was a significant and positive contributor to ASPD under both full and reduced EDF values. In all species but A. marmoreus, RYM was a significant and negative contributor to ASPD under full EDF values. That is, as a thread's extensibility was reduced, its per droplet stickiness also decreased. When EDF2 values were considered, strong support for a negative contribution of RYM remained in M. gracilis and V. arenata but there was only weak support for a negative contribution of RYM in A. aurantia and C. turbinata.
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Our failure to find a strong support for models of ASPD based on DV and RYM in A. aurantia and A. marmoreus may result from high DV variance in these species or to a low correlation between the DV and ASPD in the individuals that we studied. The relationships between DV and ASPD for the unstretched threads of A. aurantia and A. marmoreus were not significant (P=0.1327 and 0.1859, respectively) whereas this relationship was significant for M. gracilis, V. arenata and C. turbinata (P=0.0038, P=0.0061 and 0.0303, respectively).
We used the significant regression models for M. gracilis, V. arenata and C. turbinata to illustrate graphically the contributions of RYM and DV to ASPD (Fig. 7). These models showed that, as threads are elongated, the adhesion attributed to droplet volume alone increasingly exceeded measured ASPD whereas increasing amounts of potential adhesion are lost to reduced thread extensibility.
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Assessing the effects of stress relaxation
When a polymer is elongated and maintained in this strained condition, the
resulting stress can cause the fiber to lengthen, thereby reducing this
stress. This behavior is known as stress relaxation and was demonstrated
(Denny, 1976) to occur in the
viscous threads of Araneus sericatus. When these threads were
strained to 262% of their initial length (87% of their breaking elongations),
they registered a stress of 18.65 Nm–2. Within 10
min, this stress diminished to 18.37 Nm–2 (52% of
their initial stress) and after 38 min they achieved stress equilibrium at a
value that was only slightly less [fig. 11 in Denny
(Denny, 1976)]. When
interpreted in light of the stress–strain curve of this species' viscous
threads [fig. 9 in Denny (Denny,
1976)], this shows that, after undergoing stress relaxation, the
effective strain of these threads was 227% rather than the initial 262% that
they experienced. Thus, if the stress–strain curve of the stress-relaxed
thread was unaltered, it appears that stress relaxation restored 13% of the
thread's residual elongation and reduced the thread's Young's modulus. The
Young's modulus of threads at rupture was 0.367, and at an elongation of 262%
it was 0.179. If the stress–strain curve of the stress-relaxed thread
was unaltered, the Young's modulus would be 0.115. These values translate into
RYM values of 1.00, 0.49 and 0.31, respectively. However, the
stress–strain curves of stress-relaxed threads almost certainly have
steeper slopes than those of native threads.
The time required to screen and photograph threads before measuring their stickiness allowed all of the threads used in this study to reach their stress relaxation equilibriums. This means that the residual extensibility of all of the stretched threads was probably greater than our indices of relative Young's modulus indicate and was probably proportionately greater for threads that were stretched to a higher percentage of their breaking elongations. The mean realized 3x extensions of the threads of M. gracilis, A. marmoreus, A. trifasciata, C. turbinata and V. arenata, expressed as a percentage of their mean breaking extensions, were 30%, 43%, 47%, 47% and 75%, respectively. Thus, stress relaxation should have had the most pronounced effect on stretched threads of V. arenata.
To assess this effect, we performed an additional regression for V. arenata threads using reduced RYM values computed from the data on A. sericatus. Relative to breaking elongation, the 3x elongation of V. arenata threads was 86% that of A. sericatus. As the stress-relaxed RYM of A. sericatus threads was 37% less than their elongated RYM, this translates to a 32% reduction in the RYM values of 3x V. arenata threads. The mean realized 2x extension of V. arenata threads was 53% of their mean breaking extensions. If the RYM of a stress-relaxed thread decreases in proportion to its elongation, then the values of a 2x thread should be 71% that of a 3x thread or 23% that of thread that has not undergone stress relaxation. The regression model based on these modified RYM values is significant (Model P EDF1=0.0001, DV P EDF1=0.0001, RYM DV P EDF1=0.0125) and shows that ASPD is directly related to DV and inversely related to RYM (ASPD=0.001DV–8.923RYM+13.529).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Our attempt to evaluate the effect of stress relaxation on stretched threads used the conservative assumption that the slope of the stress–strain curve of stress-relaxed threads is identical to that of threads that have not undergone stress relaxation. Nonetheless, it confirmed that thread extensibility contributes positively to the stickiness of V. arenata threads, which were elongated to a much greater percentage of their breaking lengths than were threads of the other species. Consequently, we believe that stress relaxation did not confound the broader conclusions of our study. A complete explanation of viscous thread performance must incorporate this phenomenon, although the preliminary calculations that we present suggest that this will be challenging.
The molecular structure of silk affects its mechanical properties
(Hayashi et al., 1999; Hayashi
et al., 2001; Hayashi et al.,
2004; Hayashi and Lewis,
2001; Craig, 2003;
Ayoub et al., 2007) and appears
to explain intraspecific (Blackledge and
Hayashi, 2006) and interspecific
(Swanson et al., 2006a;
Swanson et al., 2006b)
differences in thread properties. However, the observed 2.5-fold difference
among the breaking factors of the five species' viscous threads
(Table 1) cannot be attributed
solely to differences in the molecular composition of their axial fibers. As
we measured threads at their native, in-web tensions and did not standardize
their tensions prior to measuring their breaking factors, we were unable to
factor out the contribution that differences in web construction behavior may
have made to the observed differences in thread breaking factors. Members of
some species may stretch their capture threads more than others before they
attach them to the web's radial lines. If they do, then a greater portion of
the potential extensibility of these threads would have been expended, leaving
them with less usable extensibility.
The mean 33.9% lost adhesion that can be attributed to reduced
extensibility in the 3x stretched threads documents the important
contribution that thread extensibility makes to thread stickiness. Threads of
all species could be elongated more than the realized 3x extensions on
which this estimate was based. However, this 33.9% is probably a reasonable
estimate of the typical contribution of axial fiber extensibility to thread
adhesion because features of orb-web architecture constrain the elongation
that viscous threads undergo when intercepting and retaining prey. Insects
usually strike multiple spiral turns, thereby distributing impact forces and
struggling stresses over several thread spans. Moreover, aerodynamic dampening
helps vertical orb-webs absorb the forces of prey impact as webs flex through
the air (Lin et al., 1995).
Even this web flexibility is constrained by the combined extensibility of the
web's radial and capture lines (Craig,
1987; Craig,
2003).
Intraspecific differences in droplet volume, droplet spacing and maximum thread extensibility made it challenging to evaluate the contribution of axial fiber extensibility to thread adhesion. Only by accounting for each of these variables was it possible to document the role of axial fiber extensibility in thread adhesion. Interspecific differences in maximum thread extensibility and stickiness per droplet volume made it impossible to develop a more general model that describes the performance of the five species' threads. This may indicate that each species' capture threads comprise a unique and highly tuned system whose performance integrates the axial fiber's native extensibility, the extensibility realized after the thread is deposited in a web, the thread's droplet spacing, and the adhesion and plasticity of individual thread droplets.
LIST OF ABBREVIATIONS
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Acknowledgments |
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